Along with the increased interest in and volume of social cognition research, there has been higher awareness of a lack of agreement on the concepts and taxonomy used to study social processes. Two ...central concepts in the field, empathy and Theory of Mind (ToM), have been identified as overlapping umbrella terms for different processes of limited convergence. Here, we review and integrate evidence of brain activation, brain organization, and behavior into a coherent model of social-cognitive processes. We start with a meta-analytic clustering of neuroimaging data across different social-cognitive tasks. Results show that understanding others' mental states can be described by a multilevel model of hierarchical structure, similar to models in intelligence and personality research. A higher level describes more broad and abstract classes of functioning, whereas a lower one explains how functions are applied to concrete contexts given by particular stimulus and task formats. Specifically, the higher level of our model suggests 3 groups of neurocognitive processes: (a) predominantly cognitive processes, which are engaged when mentalizing requires self-generated cognition decoupled from the physical world; (b) more affective processes, which are engaged when we witness emotions in others based on shared emotional, motor, and somatosensory representations; (c) combined processes, which engage cognitive and affective functions in parallel. We discuss how these processes are explained by an underlying principal gradient of structural brain organization. Finally, we validate the model by a review of empathy and ToM task interrelations found in behavioral studies.
Public Significance Statement
Empathy and Theory of Mind are important human capacities for understanding others. Here, we present a meta-analysis of neuroimaging data from 4,207 participants, which shows that these abilities can be deconstructed into specific and partially shared neurocognitive subprocesses. Our findings provide systematic, large-scale support for the hypothesis that understanding others' mental states can be described by a multilevel model of hierarchical structure, similar to models in intelligence and personality research.
•Comparing species can provide insights into the evolutionary history.•Comparative neuroimaging allow to access in vivo anatomy and cognition.•Access to more data across species will soon allow us to ...model the brains of common ancestors.•Comparative neuroimaging may help discover neuroprotective mechanisms.
Evolution, as we currently understand it, strikes a delicate balance between animals' ancestral history and adaptations to their current niche. Similarities between species are generally considered inherited from a common ancestor whereas observed differences are considered as more recent evolution. Hence comparing species can provide insights into the evolutionary history. Comparative neuroimaging has recently emerged as a novel subdiscipline, which uses magnetic resonance imaging (MRI) to identify similarities and differences in brain structure and function across species. Whereas invasive histological and molecular techniques are superior in spatial resolution, they are laborious, post-mortem, and oftentimes limited to specific species. Neuroimaging, by comparison, has the advantages of being applicable across species and allows for fast, whole-brain, repeatable, and multi-modal measurements of the structure and function in living brains and post-mortem tissue. In this review, we summarise the current state of the art in comparative anatomy and function of the brain and gather together the main scientific questions to be explored in the future of the fascinating new field of brain evolution derived from comparative neuroimaging.
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Fifteen years ago, Passingham and colleagues proposed that brain areas can be described in terms of their unique pattern of input and output connections with the rest of the brain, and that these ...connections are a crucial determinant of their function. We explore how the advent of neuroimaging of connectivity has allowed us to test and extend this proposal. We show that describing the brain in terms of an abstract connectivity space, as opposed to physical locations of areas, provides a natural and powerful framework for thinking about brain function and its variation across the brains of individuals, populations, and species.
The concept of the connectivity fingerprint was described 15 years ago to suggest a crucial relationship between the connections (functional integration) and function (functional segregation) of an area.
The advent of neuroimaging now allows for this concept to be applied on a much larger scale, describing brain organization in terms of a connectivity space.
Describing brain organization in this space is closer to its functional organization and can predict differences in functional activation and behaviour.
By abstracting away into connectivity space one can compare brains across individuals and species.
Comparing differences in the connectivity fingerprints of areas or subareal units in terms of gradients, one can investigate which dimension of connectivity space is relevant for understanding particular aspects of brain organization.
Reward-guided decision-making depends on a network of brain regions. Among these are the orbitofrontal and the anterior cingulate cortex. However, it is difficult to ascertain if these areas ...constitute anatomical and functional unities, and how these areas correspond between monkeys and humans. To address these questions we looked at connectivity profiles of these areas using resting-state functional MRI in 38 humans and 25 macaque monkeys. We sought brain regions in the macaque that resembled 10 human areas identified with decision making and brain regions in the human that resembled six macaque areas identified with decision making. We also used diffusion-weighted MRI to delineate key human orbital and medial frontal brain regions. We identified 21 different regions, many of which could be linked to particular aspects of reward-guided learning, valuation, and decision making, and in many cases we identified areas in the macaque with similar coupling profiles.
Significance Because of the interest in reward-guided learning and decision making, these neural mechanisms have been studied in both humans and monkeys. But whether and how key brain areas correspond between the two species has been uncertain. Areas in the two species can be compared as a function of the brain circuits in which they participate, which can be estimated from patterns of correlation in brain activity measured with functional MRI. Taking such measurements in 38 humans and 25 macaques, we identified fundamental similarities between the species and one human frontal area with no monkey counterpart. Altogether these findings suggest that everyday human decision-making capitalizes on a neural apparatus similar to the one that supports monkeys when foraging in the wild.
The causal role of an area within a neural network can be determined by interfering with its activity and measuring the impact. Many current reversible manipulation techniques have limitations ...preventing their application, particularly in deep areas of the primate brain. Here, we demonstrate that a focused transcranial ultrasound stimulation (TUS) protocol impacts activity even in deep brain areas: a subcortical brain structure, the amygdala (experiment 1), and a deep cortical region, the anterior cingulate cortex (ACC, experiment 2), in macaques. TUS neuromodulatory effects were measured by examining relationships between activity in each area and the rest of the brain using functional magnetic resonance imaging (fMRI). In control conditions without sonication, activity in a given area is related to activity in interconnected regions, but such relationships are reduced after sonication, specifically for the targeted areas. Dissociable and focal effects on neural activity could not be explained by auditory confounds.
•Ultrasound stimulation exerts regionally specific neural effects in primates•It can be used to alter activity even in subcortical and deep cortical areas•After stimulation, activity in a brain area is less related to that of its network•The effect lasted for more than 1 h and was not mediated by auditory confounds
Ultrasound can be used to modulate activity in deep brain areas. After stimulation, activity in the targeted brain area becomes less coupled to its network. Effects are specific to the stimulation site, long-lasting, and not due to auditory confounds.
The default mode network (DMN) of the brain consists of areas that are typically more active during rest than during active task performance. Recently however, this network has been shown to be ...activated by certain types of tasks. Social cognition, particularly higher-order tasks such as attributing mental states to others, has been suggested to activate a network of areas at least partly overlapping with the DMN. Here, we explore this claim, drawing on evidence from meta-analyses of functional MRI data and recent studies investigating the structural and functional connectivity of the social brain. In addition, we discuss recent evidence for the existence of a DMN in non-human primates. We conclude by discussing some of the implications of these observations.
We present a new software package with a library of standardised tractography protocols devised for the robust automated extraction of white matter tracts both in the human and the macaque brain. ...Using in vivo data from the Human Connectome Project (HCP) and the UK Biobank and ex vivo data for the macaque brain datasets, we obtain white matter atlases, as well as atlases for tract endpoints on the white-grey matter boundary, for both species. We illustrate that our protocols are robust against data quality, generalisable across two species and reflect the known anatomy. We further demonstrate that they capture inter-subject variability by preserving tract lateralisation in humans and tract similarities stemming from twinship in the HCP cohort. Our results demonstrate that the presented toolbox will be useful for generating imaging-derived features in large cohorts, and in facilitating comparative neuroanatomy studies. The software, tractography protocols, and atlases are publicly released through FSL, allowing users to define their own tractography protocols in a standardised manner, further contributing to open science.
•A new software package for standardised and automated cross-species tractography.•Homologous white matter bundles in the human and macaque brain.•Human white matter tract atlases generated from large datasets (1000 subjects).•Tractography protocols are standardised, but preserve individual variability.•Generalisability across datasets shown using the HCP and the UK Biobank data.
Dorsal anterior cingulate cortex (dACC) carries a wealth of value-related information necessary for regulating behavioral flexibility and persistence. It signals error and reward events informing ...decisions about switching or staying with current behavior. During decision-making, it encodes the average value of exploring alternative choices (search value), even after controlling for response selection difficulty, and during learning, it encodes the degree to which internal models of the environment and current task must be updated. dACC value signals are derived in part from the history of recent reward integrated simultaneously over multiple time scales, thereby enabling comparison of experience over the recent and extended past. Such ACC signals may instigate attentionally demanding and difficult processes such as behavioral change via interactions with prefrontal cortex. However, the signal in dACC that instigates behavioral change need not itself be a conflict or difficulty signal.
The temporal association cortex is considered a primate specialization and is involved in complex behaviors, with some, such as language, particularly characteristic of humans. The emergence of these ...behaviors has been linked to major differences in temporal lobe white matter in humans compared with monkeys. It is unknown, however, how the organization of the temporal lobe differs across several anthropoid primates. Therefore, we systematically compared the organization of the major temporal lobe white matter tracts in the human, gorilla, and chimpanzee great apes and in the macaque monkey. We show that humans and great apes, in particular the chimpanzee, exhibit an expanded and more complex occipital-temporal white matter system; additionally, in humans, the invasion of dorsal tracts into the temporal lobe provides a further specialization. We demonstrate the reorganization of different tracts along the primate evolutionary tree, including distinctive connectivity of human temporal gray matter.
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